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Predation on Endangered Species by Human-Subsidized Domestic Cats On www.nature.com/scientificreports OPEN Predation on endangered species by human-subsidized domestic cats on Tokunoshima Island Tamao Maeda1, Rumiko Nakashita2, Kazumi Shionosaki3,4, Fumio Yamada2 & Yuya Watari 2* It is important to unravel how invasive species impact native ecosystems in order to control them efectively. The presence of abundant exotic prey promotes population growth of invasive predators, thereby enhancing the predation pressure on native prey (hyper-predation). Not only the exotic prey but also feeding by humans is likely to cause “hyper-predation”. However, the contribution of artifcial resources to this was underestimated in previous studies. Here, we combined fecal and stable isotope analyses to reveal short- and long-term food habits of free-ranging cats on Tokunoshima Island. Although 20.1% of the feral cat feces contained evidence of forest-living species, stable isotope analysis suggested that the cats were mostly dependent on artifcial resources. In addition, a general linear model analysis showed that their diet was strongly correlated with landscape variables. These results indicate that the invasive free-ranging cats are aided by anthropogenic feeding, and they move from the human habituated area to natural areas with high biodiversity. These fndings suggest the possibility of human feeding indirectly accelerates the efect of cat predation, and call for a further study on their demography. Cat management mainly involves trapping, but our fndings show that educating local residents to stop feeding free-ranging cats and keeping pet cats indoors are also important. Biological invasion is one of the major causes of biodiversity loss globally1,2, especially in insular ecosystems worldwide3,4. To efectively control invasive species, it is important to determine how they survive and increase their populations in the areas that they invade. Te establishment of populations is one of the essential processes for successful invasion5,6; in other words, the impact of the introduced species may not become evident unless they have succeeded in increasing their numbers7,8. Various factors, such as species traits, biotic and abiotic envi- ronments, and temporal events, can afect a result of such establishment, subsequent increases in abundance, and the ecological impact of an invasive species8,9. Hyper-predation is one of the possible processes enhancing the impact of invasive predators10. Tis hypothesis predicts that the presence of abundant primary prey subsidizes the predator population, allowing it to grow and then more severely impact the relatively scarce native prey11,12. Feral cats (Felis catus) are among the most infuential introduced species13, as they have been responsible for the extinction or decrease in numerous mammals, birds, and reptiles, particularly in insular ecosystems13–19. Many studies have reported that introduced prey (e.g., European rabbits, black rats, and house mice) are sus- pected of causing hyper-predation to feral cats on native organisms11,18,20. Te most well-known example is the case on Macquarie Island, where invasive feral cats caused extinction of the endemic parakeet, Cyanoramphus novaezelandiae erythrotis7. Feral cats and parakeets coexisted on the island for 60 years, but afer rabbits were introduced, feral cats rapidly increased their number and ate up the parakeets in the next 10 years. Not only the introduced prey but also direct or indirect feeding by humans support cat populations and enhance predation pressure on native species, thereby accelerating their extinction10,21–23. Some previous studies reported that cats fed by people can substantially impact on the local ecosystem21,24. However, most of the studies were limited to native predators living in urban or peri-urban areas23. Tokunoshima Island is located in southwestern Japan and is a biodiversity hotspot with unique biota that evolved in the absence of native mammalian predators25. On this island and adjacent Amami-Oshima and Okinawa Island, free-ranging cats prey on endangered endemic species, such as Amami rabbit (Pentalagus fur- nessi), Ryukyu long-haired rat (Diplothrix legata), and spiny rat (Tokudaia tokunoshimensis, T. osimensis and 1Wildlife Research Center, Kyoto University, 2-24 Tanaka-Sekiden-cho, Sakyo, Kyoto, 606-8203, Japan. 2Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan. 3Amami Wild Animal Research Center, 2662 Ogachi, Tatsugo-cho, Kagoshima, 894-0105, Japan. 4Amami Wildlife Research Center Co., Ltd, 10-11-2F Naze Suehiro-cho, Amami, Kagoshima, 894-0027, Japan. *email: [email protected] SCIENTIFIC REPORTS | (2019) 9:16200 | https://doi.org/10.1038/s41598-019-52472-3 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. Feral cats killing endemic mammals taken by censor cameras on Tokunoshima Island. (a) Amami rabbit, (b) Ryukyu long-haired rat. (a) Photograph was taken in 2017 and provided with permission by the Naha Nature Conservation Ofce, Ministry of the Environment. (b) Photograph taken in 2018 by the author (Y. Watari, Forestry and Forest Products Research Institute). T. muenninki)26,27, and are believed to be responsible for the population reduction of these species on the islands28,29 (Fig. 1). Indeed, a camera-trapping study by the Japanese Ministry of the Environment found a neg- ative correlation between the number of cat appearances and that of endangered Amami rabbits, indicating that the presence of cats can limit the rabbit distribution30. Te local Tokunoshima Island government and the Ministry of the Environment have been capturing free-ranging cats since 2014 to conserve the endemic species. Cats caught in forests are referred to here as “feral” cats, whereas those caught in residential areas or farmlands are called “stray” cats. “Feral” cats are kept in a shelter, and some can be adopted by new owners afer sterilization, whereas “stray” cats are returned to the wild afer sterilization (TNR) because it is implicitly assumed that they do not enter the forest and prey on native animals. Tis management program has been achieving some degree of success, as the monthly route census conducted by the Ministry of the Environment showed that the encounter rates of three endangered mammals, Amami rabbits, Tokunoshima spiny rats (T. tokunoshimensis), and Ryukyu long-haired rats, have been increasing while that of cats are decreasing since 201431. It has also been suggested that free-ranging cats are placing substantial predation pressure on native species. Scientifcally, the term “feral” means completely independent and rarely interacting with humans, whereas “stray” cats do not have an owner but still depend on human care32. Te division of “feral” and “stray” cats by the government suggests their assumption that cats rarely migrate between forests and residential areas, but it is still unclear whether this division is scientifcally appropriate due to the lack of studies on free-ranging cats on Tokunoshima Island. Tokunoshima Island is characterized by small forested areas33, so it is rather likely that “feral” cats and “stray” cats have access to both wild animals in the forest and artifcial food in the villages. Even the core area of the forest is only a few kilometers away from farmlands, which is close enough for free-ranging cats to access both34–37. Human garbage was found in 7.1–50% of cat feces on the northern part of Okinawa Island (Yambaru) and Amami-Oshima Islands26,27. However, fecal analysis cannot be used for accurate estimation of the actual dependence on artifcial resources, owing to the diferent digestibility among food items38. Instead, stable isotope analysis is a powerful method to clarify the dependence of subjects on a given food item39. If the so-called “feral” cats are fed with human food, in order to reduce the high predation on native species, it could be efective to keep domestic cats indoors or stop feeding cats without owners. Evidence of resource dependence of cats would provide strong support in promoting public awareness of this issue and in developing an efective strategy for conserving native species. Tis study evaluated the diet of free-ranging cats on Tokunoshima Island to verify our hypothesis that both “feral” and “stray” cats are accessible to the forest and the residential area and they are highly dependent on the human-provided resources, although they also predate endemic species in the forest. Tis dietary state of cats is one of the necessary conditions for the occurrence of hyper-predation induced by human-derived food resources. We specifcally addressed three questions: (1) Do “feral” cats eat endangered species more ofen than “stray” cats? (2) Does providing artifcial food substantially support diet of free-ranging cats? (3) Do the contributions of forest prey (including endangered species) and artifcial food of free-ranging cats difer among capture locations with diferent surrounding landscapes? To answer these questions, we collected fecal and hair samples from trapped free-ranging cats and conducted fecal and stable isotope analyses. Results Fecal analysis. In total, 208 “feral” cats (75 females, 123 males, and 10 unidentifed) and 54 “stray” cats (22 females, 30 males, and 2 unidentifed) were captured, and 198 fecal samples (from 174 “feral” cats and 24 “stray” cats) were obtained (Fig. 2). A total of 13.4% of the cats (35; 31 “feral” and 4 “stray”) were ear-tipped, which means that they had been captured as “stray” cats and sterilized (Table S1). Evidence of forest-living species and farm- land-living animals were found in at least 17.7% and 30.8% of the fecal samples, respectively (Table 1). Overall, 23.7% of fecal samples contained artifcial objects, such as plastic or paper (Table 1). In addition, 20.1% of the fecal samples from “feral” cats contained evidence of forest animals, which was signifcantly higher than the rate for “stray” cats (0.0%) (Fisher’s exact test, p < 0.01). No signifcant diference was observed in the occurrence frequency of farmland species (“feral”: 31.6%, “stray”: 20.8%) and artifcial objects (“feral”: 24.1%, “stray”: 20.8%) (p > 0.05).
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